Review and prospect of transgenic rice research

Rice is one of the most important crops as the staple food for more than half of the world’s population. Rice improvement has achieved remarkable success in the past half-century, with the yield doubled in most parts of the world and even tripled in certain regions, which has contributed greatly to food security globally. Rapid population growth and economic development pose a constantly increased food requirement. However, rice yield has been hovering in the past decade, which is mainly caused by the absence of novel breeding technologies, reduction of genetic diversity of rice cultivars, and serious yield loss due to increasingly severe occurrences of insects, diseases, and abiotic stresses. To address these challenges, Chinese scientists proposed a novel rice breeding goal of developing Green Super Rice to improve rice varieties and realize the sustainable development of agriculture, by focusing on the following 5 classes of traits: insect and disease resistance, drought-tolerance, nutrient-use efficiency, quality and yield potential. As a modern breeding approach, transgenic strategy will play an important role in realizing the goal of Green Super Rice. Presently, many transgenic studies of rice have been conducted, and most of target traits are consistent with the goal of Green Super Rice. In this paper, we firstly review technical advances of rice transformation, and then outline the main progress in transgenic rice research with respect to the most important traits: insect and disease-resistance, drought-tolerance, nutrient-use efficiency, quality, yield potential and herbicide-tolerance. The prospects of developing transgenic rice are also discussed.

[1]  N. Kamasawa,et al.  Aberrant chloroplasts in transgenic rice plants expressing a high level of maize NADP-dependent malic enzyme , 2000, Planta.

[2]  B. San Segundo,et al.  The −689/+197 region of the maize protease inhibitor gene directs high level, wound-inducible expression of the cry1B gene which protects transgenic rice plants from stemborer attack , 2001, Molecular Breeding.

[3]  T. Yamaya,et al.  Assimilation of ammonium ions and reutilization of nitrogen in rice (Oryza sativa L.). , 2007, Journal of experimental botany.

[4]  Li Liu,et al.  Development of insect-resistant transgenic rice with Cry1C*-free endosperm. , 2009, Pest management science.

[5]  Adity Gupta,et al.  Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice , 2008, Plant Molecular Biology.

[6]  W. Zhang,et al.  Efficient regeneration of transgenic plants from rice protoplasts and correctly regulated expression of the foreign gene in the plants , 1988, Theoretical and Applied Genetics.

[7]  D. Shibata,et al.  Complementation of plant mutants with large genomic DNA fragments by a transformation-competent artificial chromosome vector accelerates positional cloning. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[8]  M. Matsuoka,et al.  Significant Accumulation of C4-Specific Pyruvate, Orthophosphate Dikinase in a C3 Plant, Rice , 2001 .

[9]  Jayaprakash Targolli,et al.  Wheat LEA genes, PMA80 and PMA1959, enhance dehydration tolerance of transgenic rice (Oryza sativa L.) , 2002, Molecular Breeding.

[10]  W. Sawahel Improved Performance of Transgenic Glycinebetaine-Accumulating Rice Plants under Drought Stress , 2003, Biologia Plantarum.

[11]  S. Raina,et al.  Elite Indica Transgenic Rice Plants Expressing Modified Cry1Ac Endotoxin of Bacillus Thuringiensis Show Enhanced Resistance to Yellow Stem Borer (Scirpophaga Incertulas) , 2002, Transgenic Research.

[12]  Manyuan Long,et al.  A Rice Gene of De Novo Origin Negatively Regulates Pathogen-Induced Defense Response , 2009, PloS one.

[13]  L. Xiong,et al.  Disease Resistance and Abiotic Stress Tolerance in Rice Are Inversely Modulated by an Abscisic Acid–Inducible Mitogen-Activated Protein Kinase Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.008714. , 2003, The Plant Cell Online.

[14]  M. Nam,et al.  Increased expression of OsPT1, a high-affinity phosphate transporter, enhances phosphate acquisition in rice , 2008, Biotechnology Letters.

[15]  Gurdev S. Khush,et al.  Enhanced resistance to two stem borers in an aromatic rice containing a synthetic cryIA(b) gene , 1997, Molecular Breeding.

[17]  A. Kohli,et al.  Development, field evaluation, and agronomic performance of transgenic herbicide resistant rice , 2004, Molecular Breeding.

[18]  S. Oka,et al.  Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. , 2006, The Plant journal : for cell and molecular biology.

[19]  N. Baisakh,et al.  Pyramiding transgenes for multiple resistance in rice against bacterial blight, yellow stem borer and sheath blight , 2002, Theoretical and Applied Genetics.

[20]  K. Back,et al.  Herbicidal and antioxidant responses of transgenic rice overexpressing Myxococcus xanthus protoporphyrinogen oxidase. , 2005, Plant physiology and biochemistry : PPB.

[21]  P. Christou,et al.  Enhanced insect resistance in Thai rice varieties generated by particle bombardment , 2000, Molecular Breeding.

[22]  S. Karim,et al.  Toxicity and Receptor Binding Properties of Bacillus thuringiensisδ-Endotoxins to the Midgut Brush Border Membrane Vesicles of the Rice Leaf Folders, Cnaphalocrocis medinalis and Marasmia patnalis , 2000, Current Microbiology.

[23]  Xuequn Liu,et al.  Identification and fine mapping of the new bacterial blight resistance gene, Xa31(t), in rice , 2009, European Journal of Plant Pathology.

[24]  M. Matsuoka,et al.  High level expression of C4-specific NADP-malic enzyme in leaves and impairment of photoautotrophic growth in a C3 plant, rice. , 2001, Plant & cell physiology.

[25]  B. Ney,et al.  The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. , 2007, Journal of experimental botany.

[26]  Wu Jia Study on Resistance Gene to Bacterial Blight Xa21 Transgenic Rice and Their Hybrid Combinations , 2001 .

[27]  P. Miklas,et al.  The role of RAPD markers in breeding for disease resistance in common bean , 1998, Molecular Breeding.

[28]  R. Dean,et al.  Expression of a harpin-encoding gene in rice confers durable nonspecific resistance to Magnaporthe grisea. , 2007, Plant biotechnology journal.

[29]  E. Hinchliffe,et al.  Improving the nutritional value of Golden Rice through increased pro-vitamin A content , 2005, Nature Biotechnology.

[30]  Yaoguang Liu,et al.  [Development of transformation system of rice based on transformation-competent artificial chromosome (TAC) vector]. , 2005, Yi chuan xue bao = Acta genetica Sinica.

[31]  Mayumi Tabuchi,et al.  Biochemical background and compartmentalized functions of cytosolic glutamine synthetase for active ammonium assimilation in rice roots. , 2004, Plant & cell physiology.

[32]  Suk-Yoon. Kwon,et al.  Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. , 2005, Journal of plant physiology.

[33]  M. Matsuoka,et al.  High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants , 1999, Nature Biotechnology.

[34]  Geert Plaetinck,et al.  Control of coleopteran insect pests through RNA interference , 2007, Nature Biotechnology.

[35]  P. Lucca,et al.  Genetic engineering approaches to improve the bioavailability and the level of iron in rice grains , 2001, Theoretical and Applied Genetics.

[36]  Zhi-ming Wei,et al.  Agrobacterium tumefaciens-mediated transformation of rice with the spider insecticidal gene conferring resistance to leaffolder and striped stem borer , 2001, Cell Research.

[37]  L. Xiong,et al.  Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice , 2006, Proceedings of the National Academy of Sciences.

[38]  A. Basu,et al.  Transgenic elite indica rice plants expressing CryIAc delta-endotoxin of Bacillus thuringiensis are resistant against yellow stem borer (Scirpophaga incertulas). , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[39]  H. Ohkawa,et al.  Herbicide resistance in transgenic plants with mammalian P450 monooxygenase genes. , 2005, Pest management science.

[40]  S. Riazuddin,et al.  Expression of multiple insecticidal genes confers broad resistance against a range of different rice pests , 2004, Molecular Breeding.

[41]  Wei Huang,et al.  A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase , 2007, Nature Genetics.

[42]  M. Gu,et al.  Variation and distribution of seed storage protein content and composition among different rice varieties. , 2009 .

[43]  M. Udvardi,et al.  Over-expression of the rice OsAMT1-1 gene increases ammonium uptake and content, but impairs growth and development of plants under high ammonium nutrition. , 2006, Functional plant biology : FPB.

[44]  S. Toki,et al.  Iron fortification of rice seed by the soybean ferritin gene , 1999, Nature Biotechnology.

[45]  A. Altman,et al.  Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. , 2005, Current opinion in biotechnology.

[46]  S. Kim,et al.  Arabidopsis CBF3/DREB1A and ABF3 in Transgenic Rice Increased Tolerance to Abiotic Stress without Stunting Growth1[w] , 2005, Plant Physiology.

[47]  I. Altosaar,et al.  Field Evaluation of Resistance of Transgenic Rice Containing a Synthetic cry1Ab Gene from Bacillus thuringiensis Berliner to Two Stem Borers , 2001, Journal of economic entomology.

[48]  N. P. Sarma,et al.  Development of stem borer resistant transgenic parental lines involved in the production of hybrid rice. , 2004, Journal of biotechnology.

[49]  Xin-Yao Yu,et al.  The role of aquaporin RWC3 in drought avoidance in rice. , 2004, Plant & cell physiology.

[50]  J. Gatehouse,et al.  Transgenic indica rice resistant to sap-sucking insects. , 2003, Plant Biotechnology Journal.

[51]  Wei Tang,et al.  Development of insect-resistant transgenic indica rice with a synthetic cry1C* gene , 2006, Molecular Breeding.

[52]  Kokichi Hinata,et al.  Transgenic Rice Plants After Direct Gene Transfer into Protoplasts , 1988, Bio/Technology.

[53]  Bienvenido O. Juliano,et al.  Rice : chemistry and technology , 1985 .

[54]  K. Tang,et al.  Transgenic rice lines with enhanced resistance to the small brown planthopper , 2002 .

[55]  S. Ha,et al.  Dual targeting of Myxococcus xanthus protoporphyrinogen oxidase into chloroplasts and mitochondria and high level oxyfluorfen resistance , 2004 .

[56]  Deng Xiao,et al.  LRP Transgenic Indica Rice Restorer Line without Resistance Selection Marker , 2006 .

[57]  H. Inui,et al.  Transgenic rice containing human CYP2B6 detoxifies various classes of herbicides. , 2005, Journal of agricultural and food chemistry.

[58]  D. Sudhakar,et al.  Pyramiding transgenic resistance in elite indica rice cultivars against the sheath blight and bacterial blight , 2007, Plant Cell Reports.

[59]  Takuya Fukuda,et al.  Overproduction of C4 photosynthetic enzymes in transgenic rice plants: an approach to introduce the C4-like photosynthetic pathway into rice. , 2007, Journal of experimental botany.

[60]  Xianghua Li,et al.  Over-expression of aspartate aminotransferase genes in rice resulted in altered nitrogen metabolism and increased amino acid content in seeds , 2009, Theoretical and Applied Genetics.

[61]  S. Song,et al.  Expression of a Bifunctional Fusion of the Escherichia coli Genes for Trehalose-6-Phosphate Synthase and Trehalose-6-Phosphate Phosphatase in Transgenic Rice Plants Increases Trehalose Accumulation and Abiotic Stress Tolerance without Stunting Growth1 , 2003, Plant Physiology.

[62]  R. Wu,et al.  Genetic improvement of Basmati rice for salt and drought tolerance by regulated expression of a barley Hva1 cDNA , 2002 .

[63]  W. Bingliang,et al.  Transgenic rice homozygous lines expressing GNA showed enhanced resistance to rice brown planthopper , 2001 .

[64]  Yutaka Sato,et al.  Enhanced tolerance to drought stress in transgenic rice plants overexpressing a small heat-shock protein, sHSP17.7 , 2008, Plant Cell Reports.

[65]  Ji Huang,et al.  Overexpression of a TFIIIA‐type zinc finger protein gene ZFP252 enhances drought and salt tolerance in rice (Oryza sativa L.) , 2008, FEBS letters.

[66]  A. Kohli,et al.  Expression of an engineered cysteine proteinase inhibitor (Oryzacystatin-IΔD86) for nematode resistance in transgenic rice plants , 1998, Theoretical and Applied Genetics.

[67]  C. Vance,et al.  Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. , 2003, The New phytologist.

[68]  N. Baisakh,et al.  Agrobacterium-mediated engineering for sheath blight resistance of indica rice cultivars from different ecosystems , 2000, Theoretical and Applied Genetics.

[69]  S. Prashanth,et al.  Over expression of cytosolic copper/zinc superoxide dismutase from a mangrove plant Avicennia marina in indica Rice var Pusa Basmati-1 confers abiotic stress tolerance , 2008, Transgenic Research.

[70]  Xi Chen,et al.  Evaluation of seven function-known candidate genes for their effects on improving drought resistance of transgenic rice under field conditions. , 2009, Molecular plant.

[71]  D. Chao,et al.  Toward Understanding Molecular Mechanisms of Abiotic Stress Responses in Rice , 2008, Rice.

[72]  T. G. Owens,et al.  Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[73]  G. Coruzzi,et al.  THE MOLECULAR-GENETICS OF NITROGEN ASSIMILATION INTO AMINO ACIDS IN HIGHER PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[74]  Shiping Wang,et al.  Fine genetic mapping of xa24, a recessive gene for resistance against Xanthomonas oryzae pv. oryzae in rice , 2008, Theoretical and Applied Genetics.

[75]  Wei Tang,et al.  Transgenic indica rice plants harboring a synthetic cry2A* gene of Bacillus thuringiensis exhibit enhanced resistance against lepidopteran rice pests , 2005, Theoretical and Applied Genetics.

[76]  P. Christou,et al.  Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[77]  K. Shinozaki,et al.  Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. , 2006, Plant & cell physiology.

[78]  T. Komari,et al.  Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. , 1994, The Plant journal : for cell and molecular biology.

[79]  I. Altosaar,et al.  Agrobacterium-transformed rice plants expressing synthetic cryIA(b) and cryIA(c) genes are highly toxic to striped stem borer and yellow stem borer. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[80]  Lee Sungho,et al.  Soybean Kunitz trypsin inhibitor (SKTI) confers resistance to the brown planthopper (Nilaparvata lugens Stål) in transgenic rice , 1999 .

[81]  R. Wu,et al.  Transgenic rice plants harboring an introduced potato proteinase inhibitor II gene are insect resistant , 1996, Nature Biotechnology.

[82]  H. Inui,et al.  Herbicide Metabolism and Tolerance in the Transgenic Rice Plants Expressing Human CYP2C9 and CYP2C19 , 2001 .

[83]  J. Burnell,et al.  Changes in photosynthetic carbon flow in transgenic rice plants that express C4-type phosphoenolpyruvate carboxykinase from Urochloa panicoides. , 2000, Plant physiology.

[84]  R. Wu,et al.  Stress-inducible synthesis of proline in transgenic rice confers faster growth under stress conditions than that with constitutive synthesis , 2004 .

[85]  I. Altosaar,et al.  Achieving successful deployment of Bt rice. , 2004, Trends in plant science.

[86]  Ji Huang,et al.  Expression analysis of rice A20/AN1-type zinc finger genes and characterization of ZFP177 that contributes to temperature stress tolerance. , 2008, Gene.

[87]  I. Potrykus,et al.  Genetic Engineering of Rice for Resistance to Sheath Blight , 1995, Bio/Technology.

[88]  B. Kaiser,et al.  Functional characterisation of OsAMT1.1 overexpression lines of rice, Oryza sativa. , 2006, Functional plant biology : FPB.

[89]  Qifa Zhang,et al.  Optimising the tissue culture conditions for high efficiency transformation of indica rice , 2004, Plant Cell Reports.

[90]  K. Raghothama Phosphate transport and signaling. , 2000, Current opinion in plant biology.

[91]  R. Eritja,et al.  Transgenic Rice Plants Expressing the Antifungal AFP Protein from Aspergillus Giganteus Show Enhanced Resistance to the Rice Blast Fungus Magnaporthe Grisea , 2004, Plant Molecular Biology.

[92]  Shiping Zhang,et al.  Transgenic elite Indica rice varieties, resistant to Xanthomonas oryzae pv. oryzae , 2004, Molecular Breeding.

[93]  G. An,et al.  Transgenic rice plants expressing a Bacillus subtilis protoporphyrinogen oxidase gene are resistant to diphenyl ether herbicide oxyfluorfen. , 2000, Plant & cell physiology.

[94]  L. Xiong,et al.  Characterization of Stress-Responsive CIPK Genes in Rice for Stress Tolerance Improvement1[W] , 2007, Plant Physiology.

[95]  I. Díaz,et al.  Transgenic Expression of Trypsin Inhibitor CMe from Barley in Indica and Japonica Rice, Confers Resistance to the Rice Weevil Sitophilus Oryzae , 2003, Transgenic Research.

[96]  S. Datta,et al.  Transgenic fertile japonica rice plants expressing a modified cryIA(b) gene resistant to yellow stem borer , 1997, Plant Cell Reports.

[97]  D. Verma,et al.  Overexpression of a Δ1-pyrroline-5-carboxylate synthetase gene and analysis of tolerance to water- and salt-stress in transgenic rice , 1998 .

[98]  X. Xu,et al.  Plastid transformation in the monocotyledonous cereal crop, rice (Oryza sativa) and transmission of transgenes to their progeny. , 2006, Molecules and cells.

[99]  Jia-Wei Wang,et al.  Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol , 2007, Nature Biotechnology.

[100]  P. Beyer,et al.  Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. , 2000, Science.

[101]  R. Terauchi,et al.  Overexpression of the wasabi defensin gene confers enhanced resistance to blast fungus (Magnaporthe grisea) in transgenic rice , 2002, Theoretical and Applied Genetics.

[102]  Jian-Zhou Zhao,et al.  Insect resistance management in GM crops: past, present and future , 2005, Nature Biotechnology.

[103]  I. Dutta,et al.  Transgenic rice expressing Allium sativum leaf lectin with enhanced resistance against sap-sucking insect pests , 2006, Planta.

[104]  L. Xiong,et al.  Characterization of a stress responsive proteinase inhibitor gene with positive effect in improving drought resistance in rice , 2007, Planta.

[105]  Edwin P Alcantara,et al.  Bacillus thuringiensis delta-endotoxin binding to brush border membrane vesicles of rice stem borers. , 2004, Archives of insect biochemistry and physiology.

[106]  P. Christou,et al.  A transgenic rice cell lineage expressing the oat arginine decarboxylase (adc) cDNA constitutively accumulates putrescine in callus and seeds but not in vegetative tissues , 2000, Plant Molecular Biology.

[107]  Lili Zhu,et al.  Development of transformation system of rice based on binary bacterial artificial chromosome (BIBAC) vector. , 2006, Yi chuan xue bao = Acta genetica Sinica.

[108]  H. Ohkawa,et al.  Phytoremediation of the herbicides atrazine and metolachlor by transgenic rice plants expressing human CYP1A1, CYP2B6, and CYP2C19. , 2006, Journal of agricultural and food chemistry.

[109]  Zheng-Hua Ye,et al.  Mutation of a Chitinase-Like Gene Causes Ectopic Deposition of Lignin, Aberrant Cell Shapes, and Overproduction of Ethylene Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010278. , 2002, The Plant Cell Online.

[110]  S. S. Virmani,et al.  Transgenic insect-resistant maintainer line (IR68899B) for improvement of hybrid rice , 1999, Plant Cell Reports.

[111]  Qian Qian,et al.  Map-based cloning of the ALK gene, which controls the gelatinization temperature of rice , 2003, Science in China Series C: Life Sciences.

[112]  T. Komari,et al.  Agrobacterium-mediated transformation of rice using immature embryos or calli induced from mature seed , 2008, Nature Protocols.

[113]  Y. Nishizawa,et al.  Enhanced resistance to blast (Magnaporthe grisea) in transgenic Japonica rice by constitutive expression of rice chitinase , 1999, Theoretical and Applied Genetics.

[114]  Jian-Kang Zhu,et al.  Cell Signaling during Cold, Drought, and Salt Stress Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000596. , 2002, The Plant Cell Online.

[115]  N. P. Sarma,et al.  Transgenic rice plants expressing the snowdrop lectin gene (gna) exhibit high-level resistance to the whitebacked planthopper (Sogatella furcifera) , 2004, Theoretical and Applied Genetics.

[116]  R. Frutos,et al.  Expression of a Bacillus thuringiensis cry1B synthetic gene protects Mediterranean rice against the striped stem borer , 2000, Plant Cell Reports.

[117]  Yinü Li,et al.  Establishment of a Gene Expression System in Rice Chloroplast and Obtainment of PPT-Resistant Rice Plants , 2009 .

[118]  T. Yamaya,et al.  Genetic manipulation and quantitative-trait loci mapping for nitrogen recycling in rice. , 2002, Journal of experimental botany.

[119]  Lei Wang,et al.  Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice , 2007, Planta.

[120]  S. Datta,et al.  Constitutive and tissue-specific differential expression of the cryIA(b) gene in transgenic rice plants conferring resistance to rice insect pest , 1998, Theoretical and Applied Genetics.

[121]  S. Arai,et al.  Transgenic rice established to express corn cystatin exhibits strong inhibitory activity against insect gut proteinases , 2004, Plant Molecular Biology.

[122]  Kuang Ting-yun,et al.  Transfer of lysine-rich protein gene into rice and production of fertile transgenic plants , 2001 .

[123]  M. Chan,et al.  Agrobacterium-mediated production of transgenic rice plants expressing a chimeric α-amylase promoter/β-glucuronidase gene , 1993, Plant Molecular Biology.

[124]  S. Babu,et al.  Agrobacterium-mediated transformation of indica rice with chitinase gene for enhanced sheath blight resistance , 2007, Biologia Plantarum.

[125]  Ning Tang,et al.  Characterization of OsbZIP23 as a Key Player of the Basic Leucine Zipper Transcription Factor Family for Conferring Abscisic Acid Sensitivity and Salinity and Drought Tolerance in Rice1[W][OA] , 2008, Plant Physiology.

[126]  S. Tanksley,et al.  Stable transfer of intact high molecular weight DNA into plant chromosomes. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[127]  A. Kohli,et al.  Particle-bombardment-mediated co-transformation of elite Chinese rice cultivars with genes conferring resistance to bacterial blight and sap-sucking insect pests , 1999, Planta.

[128]  Jun Xiao,et al.  OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. , 2007, Molecular plant-microbe interactions : MPMI.

[129]  A. Good,et al.  Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. , 2008, Plant biotechnology journal.

[130]  Y. Nishizawa,et al.  Characterization of transgenic rice plants over-expressing the stress-inducible β-glucanase gene Gns1 , 2004, Plant Molecular Biology.

[131]  Zhen Zhu,et al.  [Obtaining stem borer-resistant homozygous transgenic lines of Minghui 81 harboring novel cry1Ac gene via particle bombardment]. , 2002, Yi chuan xue bao = Acta genetica Sinica.

[132]  Qifa Zhang Strategies for developing Green Super Rice , 2007, Proceedings of the National Academy of Sciences.

[133]  Ping Wu,et al.  OsPTF1, a Novel Transcription Factor Involved in Tolerance to Phosphate Starvation in Rice1[w] , 2005, Plant Physiology.

[134]  J. Burnell,et al.  Carbon metabolism in transgenic rice plants that express phosphoenolpyruvate carboxylase and/or phosphoenolpyruvate carboxykinase , 2006 .

[135]  T. Ho,et al.  Expression of a Late Embryogenesis Abundant Protein Gene, HVA1, from Barley Confers Tolerance to Water Deficit and Salt Stress in Transgenic Rice , 1996, Plant physiology.

[136]  S. Datta,et al.  Enhanced photosynthesis rate in genetically engineered indica rice expressing pepc gene cloned from maize , 2007 .

[137]  F. Goto,et al.  Iron accumulation does not parallel the high expression level of ferritin in transgenic rice seeds , 2005, Planta.

[138]  Bin Han,et al.  GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein , 2006, Theoretical and Applied Genetics.

[139]  H. Ohkawa,et al.  The use of cytochrome P450 genes to introduce herbicide tolerance in crops: a review , 1999 .

[140]  S. Datta,et al.  Over-expression of the cloned rice thaumatin-like protein (PR-5) gene in transgenic rice plants enhances environmental friendly resistance to Rhizoctonia solani causing sheath blight disease , 1999, Theoretical and Applied Genetics.

[141]  A. Dhingra,et al.  Multigene engineering: dawn of an exciting new era in biotechnology. , 2002, Current opinion in biotechnology.

[142]  M. Davey,et al.  Transgenic rice plants produced by electroporation-mediated plasmid uptake into protoplasts , 1988, Plant Cell Reports.

[143]  K. Toriyama,et al.  Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter , 2008, Plant Cell Reports.

[144]  Lizhong Xiong,et al.  Over-expression of a LEA gene in rice improves drought resistance under the field conditions , 2007, Theoretical and Applied Genetics.

[145]  Cheng-yun Li,et al.  [A study on introduction of chitinase gene and beta-1,3-glucanase gene into restorer line of dian-type hybrid rice (Oryza sativa L.) and enhanced resistance to blast (Magnaporthe grisea)]. , 2003, Yi chuan xue bao = Acta genetica Sinica.

[146]  Henry Daniell,et al.  Milestones in chloroplast genetic engineering: an environmentally friendly era in biotechnology. , 2002, Trends in plant science.

[147]  M. Bharathi,et al.  Expression of snowdrop lectin (GNA) in transgenic rice plants confers resistance to rice brown planthopper. , 1998, The Plant journal : for cell and molecular biology.

[148]  Cui Hairui,et al.  Development of transgenic Bacillus thuringiensis rice resistant to rice stem borers and leaf folders. , 1998 .

[149]  Cai-guo Xu,et al.  Field performance of transgenic elite commercial hybrid rice expressing Bacillus thuringiensis δ-endotoxin , 2000, Nature Biotechnology.

[150]  P. Schweizer,et al.  Constitutive expression of the defense-related Rir1b gene in transgenic rice plants confers enhanced resistance to the rice blast fungus Magnaporthe grisea , 2000, Plant Molecular Biology.

[151]  L. Xiong,et al.  A homolog of human ski-interacting protein in rice positively regulates cell viability and stress tolerance , 2009, Proceedings of the National Academy of Sciences.

[152]  A. Klöti,et al.  Transgenic Indica Rice Breeding Line IR58 Expressing a Synthetic crylA(b) Gene from Bacillus thuringiensis Provides Effective Insect Pest Control , 1996, Bio/Technology.

[153]  Y. Li,et al.  Inheritance and expression of the cry1Ab gene in Bt (Bacillus thuringiensis) transgenic rice , 2002, Theoretical and Applied Genetics.

[154]  R. Furbank,et al.  Activity regulation and physiological impacts of maize C4-specific phosphoenolpyruvate carboxylase overproduced in transgenic rice plants , 2004, Photosynthesis Research.

[155]  L. C. Loon,et al.  The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins , 1999 .

[156]  H. Nguyen,et al.  HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection , 2004 .

[157]  T. Komari,et al.  Improved protocols for transformation of indica rice mediated by Agrobacterium tumefaciens , 2006, Plant Cell, Tissue and Organ Culture.

[158]  H. Ohkawa,et al.  Herbicide resistance of transgenic rice plants expressing human CYP1A1. , 2007, Biotechnology advances.

[159]  S. Riazuddin,et al.  Effective control of yellow stem borer and rice leaf folder in transgenic rice indica varieties Basmati 370 and M 7 using the novel δ-endotoxin cry2A Bacillus thuringiensis gene , 1998, Molecular Breeding.

[160]  M. Giroux,et al.  Wheat puroindolines enhance fungal disease resistance in transgenic rice. , 2001, Molecular plant-microbe interactions : MPMI.

[161]  Jukon Kim,et al.  Co-expression of a Modified Maize Ribosome-inactivating Protein and a Rice Basic Chitinase Gene in Transgenic Rice Plants Confers Enhanced Resistance to Sheath Blight , 2003, Transgenic Research.

[162]  P. Christou,et al.  Linear transgene constructs lacking vector backbone sequences generate transgenic rice plants which accumulate higher levels of proteins conferring insect resistance , 2002, Molecular Breeding.

[163]  V. Hilder,et al.  Constitutive expression of a cowpea trypsin inhibitor gene, CpTi, in transgenic rice plants confers resistance to two major rice insect pests , 1996, Molecular Breeding.

[164]  Xia Li,et al.  Photosynthetic characteristics and tolerance to photo-oxidation of transgenic rice expressing C4 photosynthesis enzymes , 2004, Photosynthesis Research.

[165]  A. Kohli,et al.  Transgenic rice as a system to study the stability of transgene expression: multiple heterologous transgenes show similar behaviour in diverse genetic backgrounds , 2000, Theoretical and Applied Genetics.

[166]  H. Inui,et al.  Enhanced herbicide cross-tolerance in transgenic rice plants co-expressing human CYP1A1, CYP2B6, and CYP2C19 , 2005 .

[167]  G. An,et al.  Rice Pi5-Mediated Resistance to Magnaporthe oryzae Requires the Presence of Two Coiled-Coil–Nucleotide-Binding–Leucine-Rich Repeat Genes , 2009, Genetics.

[168]  Xianghua Li,et al.  Overexpressed glutamine synthetase gene modifies nitrogen metabolism and abiotic stress responses in rice , 2009, Plant Cell Reports.

[169]  Yun Zhang,et al.  Over-expression of OsDREB genes lead to enhanced drought tolerance in rice , 2008, Biotechnology Letters.

[170]  I. Potrykus,et al.  Herbicide-resistant Indica rice plants from IRRI breeding line IR72 after PEG-mediated transformation of protoplasts , 1992, Plant Molecular Biology.

[171]  Honglin Chen,et al.  Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice , 2008, Plant Molecular Biology.

[172]  Y. Xing,et al.  Nucleotide sequence of rice waxy gene. , 1990, Nucleic acids research.

[173]  H. Ohkawa,et al.  Analysis of Substrate Specificity of Pig CYP2B22 and CYP2C49 towards Herbicides by Transgenic Rice Plants , 2005, Transgenic Research.

[174]  Y. Saijo,et al.  Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. , 2000, The Plant journal : for cell and molecular biology.

[175]  M. Vasconcelos,et al.  Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene , 2003 .

[176]  P. Christou,et al.  Resistance to green leafhopper (Nephotettix virescens) and brown planthopper (Nilaparvata lugens) in transgenic rice expressing snowdrop lectin (Galanthus nivalis agglutinin; GNA). , 2000, Journal of insect physiology.

[177]  K. Osakabe,et al.  Molecular breeding of a novel herbicide-tolerant rice by gene targeting. , 2007, The Plant journal : for cell and molecular biology.

[178]  Chengcai Chu,et al.  OsMT1a, a type 1 metallothionein, plays the pivotal role in zinc homeostasis and drought tolerance in rice , 2009, Plant Molecular Biology.

[179]  P. Christou,et al.  Production of Transgenic Rice (Oryza Sativa L.) Plants from Agronomically Important Indica and Japonica Varieties via Electric Discharge Particle Acceleration of Exogenous DNA into Immature Zygotic Embryos , 1991, Bio/Technology.

[180]  K. Shimamoto,et al.  Insect Resistant Rice Generated by Introduction of a Modified δ-endotoxin Gene of Bacillus thuringiensis , 1993, Bio/Technology.

[181]  X. Cheng Agrobacterium-transformed rice plants expressing synthetic cry1Ab and cry1Ac genes are highly toxic to yellow stem borer and striped stem borer , 1998 .